Red Fox as Sentinel for Blastomyces dermatitidis, Ontario, Canada

Nicole M. Nemeth, G. Douglas Campbell, Ontario), during 1998–2014; at 2 private diagnostic servic- Paul T. Oesterle, Lenny Shirose, es (Guelph) during 1996–2006; and at the Canadian Wild- Beverly McEwen, Claire M. Jardine life Health Cooperative (Ontario regional center) during 1991–2014. Case data included date of sample collection, Blastomyces dermatitidis, a fungus that can cause fatal infec- species, and location of carcass (wildlife) or veterinary tion in humans and other mammals, is not readily recover- clinic or diagnostic laboratory (companion animals). Per- able from soil, its environmental reservoir. Because of the red sonal privacy legislation in Canada prevented use of home fox’s widespread distribution, susceptibility to B. dermatitidis, close association with soil, and well-defined home ranges, addresses for companion animals. We compared animal this animal has potential utility as a sentinel for this fungus. blastomycosis data with those for 309 published human cases in Ontario during 1994–2003 (2). Diagnoses in companion animals were made using im- lastomyces dermatitidis (family Ajellomycetaceae) is a pression smears, cytology, histopathology, serology (agar Bfungal pathogen that causes blastomycosis, a life-threat- gel immunodiffusion test), and antigen detection (sandwich ening disease in humans, canids, and other mammals (1,2). In- enzyme immunoassay). Diagnoses in wildlife were made fection usually occurs through inhalation of conidia released postmortem by gross pathology and histopathology. from an environmental reservoir (soil) (3). In North America, Blastomycosis was diagnosed in 250 companion ani- high incidences of infection are reported in humans and dogs mals (222 dogs [88.8%], 27 cats [10.8%], 1 ferret [0.4%]) from around the Great Lakes (4). Recently, increased num- and in 14 wild canids (11 red foxes [Vulpes vulpes; 78.6%], bers of human blastomycosis cases have been detected in the 3 gray wolves [Canis lupus; 21.4%]). Diagnoses in wild provinces of Quebec, Saskatchewan, Manitoba, and Ontario, canids represent 7.4% of 149 red foxes and 1.6% of 185 Canada (2,5–7). Despite this increased detection, human wolves submitted to the Canadian Wildlife Health Coop- blastomycosis is probably underdiagnosed (2,8). erative (Ontario regional center) during the same period. The geographic range of B. dermatitidis is based on Lungs of wild canids with blastomycosis consistently had reported clinical human cases and is therefore not clearly nodules of inflammatory cells and B. dermatitidis yeasts. defined 4 ( ). B. dermatitidis is not readily recoverable or Less commonly, lymph nodes and skin were also affected. uniformly distributed within the environment, and identi- In red foxes found dead, B. dermatitidis was associated fication has been problematic 4( ,9). Therefore, identifying with severe, multifocal to coalescing, granulomatous pneu- high-risk areas for exposure has been difficult, yet this this monia, whereas trapper-killed red foxes had small numbers information is crucial to minimize the number of infections. of well-circumscribed pulmonary lesions. We evaluated the utility of wild and domestic canids Most infected companion animals were from central as potential sentinels of B. dermatitidis in the environment. regions of Ontario, as previously defined 2( ); however, all We retrospectively reviewed blastomycosis case data for regions were represented (Figure). All infected wild canids wildlife and companion animals in Ontario, which contains were in the north region, where most human blastomyco- areas where blastomycosis is endemic and areas of likely sis cases (61%; 188/309) originated during 1994–2003 (2). emergence (2,3,5,8). Once a candidate sentinel species is An additional study traced 74% (20/27) of human cases to identified, a targeted surveillance system can be developed north and east of Lake Superior (3). to identify high-risk areas and assess risk factors associated Dogs were most commonly diagnosed with blastomy- with disease. cosis (64.4%) during July–December; the fewest (14%) were diagnosed during January–March. Most wildlife with The Study blastomycosis (85.7%, 10/11 red foxes and 2/3 wolves) We analyzed blastomycosis cases diagnosed at the were diagnosed during November–March; the remain- Animal Health Laboratory, University of Guelph (Guelph, ing 2 animals were diagnosed in September and April. Most human cases (59%, 181/309) were diagnosed during Author affiliations: Canadian Wildlife Health Cooperative, Guelph October–March (2). (N.M. Nemeth, G.D. Campbell, P.T. Oesterle, L. Shirose, B. dermatitidis infections in humans and other mam- C.M. Jardine); University of Guelph, Guelph, Ontario, Canada mals are opportunistic and associated with contact with (N.M. Nemeth, P.T. Oesterle, B. McEwen, C.M. Jardine) aerosolized conidia. Habitat sharing among humans, wild- DOI: http://dx.doi.org/10.3201/eid2207.151789 life, and domestic animals is increasingly common (10)

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Figure. Locations of wild and domestic canids infected with Blastomyces dermatitidis during 1996–2014, Ontario, Canada. Inset map shows the location of Ontario in Canada. Health regions within the province consist of grouped public health units as defined by the Ontario Ministry of Public Health and are named according to Morris et al. (2). Dark gray shading indicates lakes; the Great Lakes are shown in the lower part of the figure. and provides communal opportunities for B. dermatitidis probably increases the likelihood of their close and continu- exposure. Wildlife with limited and relatively well-defined ous exposure to B. dermatitidis in the soil. In addition, soil home ranges (e.g., the red fox) offer a unique opportunity in red fox dens is often sandy and acidic, a condition that, to assess the distribution and, therefore, the potential risks along with moisture, decaying vegetation, and animal feces, of exposure to pathogens with an environmental reservoir. is conducive to B. dermatitidis growth (1,3,11). The red fox is the most widely distributed carnivore Based on the co-occurrence of clinical disease in dogs worldwide and is common throughout much of North Amer- and their owners, canine blastomycosis cases are a poten- ica, including regions with endemic as well as emerging B. tial epidemiologic marker for the risk for human disease dermatitidis (11). This species is highly adaptive and coex- (9). However, in our study, pinpointing environmental ex- ists with humans in various habitats, including recreational, posure sources for dogs was impossible due to undisclosed residential, commercial, industrial, and urban open areas travel, privacy legislation, and location variation between (10). Furthermore, the home range of the red fox is compact, exposure sites and clinics. The time lag between exposure nonoverlapping, and relatively well-defined with year-round and disease onset can vary by months (13), further hin- occupancy, unlike the range of other wild canids (10,12), hu- dering accurate identification of exposure sources. In our mans, and dogs, which can have varied and long-distance study, dog blastomycosis cases mapped to Guelph are over- movements. The close proximity of red foxes to the ground, represented because this southwestern Ontario city has a along with their digging, denning, and foraging behaviors, large veterinary hospital and diagnostic laboratory.

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Although relatively few wild, compared with domes- Colleagues at the Ministry of Natural Resources and Forestry, tic, canids were diagnosed with blastomycosis in our study, Kenora District; Parks Canada; Pukaskwa National Park; and the utility of an abundant and widespread wild canid such Ministry of Natural Resources and Forestry, Parry Sound, as the red fox as a sentinel for the risk for B. dermatiti- Ontario, Canada, coordinated early wildlife submissions. dis infection in humans should be further explored. In our Dr. Nemeth is an assistant professor in the Department of study, B. dermatitidis was readily detected by gross pathol- Pathobiology at the University of Guelph. Her research interests ogy and histopathology in the lungs of red foxes, in which include vectorborne disease ecology and wildlife and pulmonary lesions ranged from severe, diffuse pneumonia zoonotic diseases. in foxes found dead to focal and well-circumscribed lesions in trapper-killed foxes. These findings suggest that B. der- matitidis–associated lesions in red foxes would be easily References identifiable, regardless of time of year and disease manifes- 1. Kerl ME. Update on canine and feline fungal diseases. Vet Clin North Am Small Anim Pract. 2003;33:721–7. http://dx.doi.org/ tation. Future sampling should target foxes in northern On- 10.1016/S0195-5616(03)00035-4 tario, where risk for human infections is highest, the annual 2. Morris SK, Brophy J, Richardson SE, Summerbell R, Parkin PC, incidence is increasing, and diagnostic testing is less avail- Jamieson F, et al. Blastomycosis in Ontario, 1994–2003. Emerg able (2,8,14). Furthermore, in remote northern regions, Infect Dis. 2006;12:274–9. http://dx.doi.org/10.3201/ eid1202.050849 defining the range and prevalence of blastomycosis could 3. Kane J, Righter J, Krajden S, Lester RS. Blastomycosis: a new have positive public health effects on healthcare workers endemic focus in Canada. Can Med Assoc J. 1983;129:728–31. and indigenous human populations. 4. Reed KD, Meece JK, Archer JR, Peterson AT. Ecologic niche Limitations for using wildlife for passive disease sur- modeling of Blastomyces dermatitidis in Wisconsin. PLoS ONE. 2008;3:e2034. http://dx.doi.org/10.1371/journal.pone.0002034 veillance include difficulty in finding and recovering car- 5. Lester RS, DeKoven JG, Kane J, Simor AE, Krajden S, casses, leading to inconsistent sampling efforts. To circum- Summerbell RC. Novel cases of blastomycosis acquired in Toronto, vent the limitations, we suggest using carcasses of licensed Ontario. CMAJ. 2000;163:1309–12. fur trapper–killed red foxes for testing in targeted areas 6. Litvinov IV, St-Germain G, Pelletier R, Paradis M, Sheppard DC. Endemic human blastomycosis in Quebec, Canada, 1988–2011. and seasons (i.e., fall to early spring). Red fox trapping is Epidemiol Infect. 2013;141:1143–7. http://dx.doi.org/10.1017/ permitted year-round in southern Ontario and from Sep- S0950268812001860 tember to late February in the remainder of the province 7. Davies JL, Epp T, Burgess HJ. Prevalence and geographic (15). Temporal detections of blastomycosis in humans in distribution of canine and feline blastomycosis in the Canadian prairies. Can Vet J. 2013;54:753–60. Ontario (2) more closely followed detections in red foxes 8. Dalcin D, Ahmed Z. Blastomycosis in northwestern Ontario, 2004 than in dogs. to 2014. Can J Infect Dis Med Microbiol. 2015;26:259–62. 9. MacDonald PDM, Langley RL, Gerkin SR, Torok MR, Conclusions MacCormack JN. Human and canine pulmonary blastomycosis, North Carolina, 2001–2002. Emerg Infect Dis. 2006;12:1242–4. Documenting the prevalence, distribution, seasonality, and http://dx.doi.org/10.3201/eid1708.050781 disease manifestations of blastomycosis in red foxes in 10. Rosatte R, Allan M. The ecology of red foxes, Vulpes vulpes, in southern Ontario could help elucidate the epidemiology of metropolitan Toronto, Ontario: disease management implications. this regionally emerging disease, delineate geospatial dif- Can Field Nat. 2009;123:215–20. 11. Lariviere S, Pasitschniak-Arts M. Vulpes vulpes. Mammalian ferences in exposure risks, and explore the utility of this Species. 1996;537:1–11. http://dx.doi.org/10.2307/3504236 wild canid as a sentinel for the risk to public health. Multi- 12. Trewhella WJ, Harris S, McAllister FE. Dispersal distance, home disciplinary research such as this provides opportunities for range size and population density in the red fox (Vulpes vulpes): the development of partnerships among public health and a quantitative analysis. J Appl Ecol. 1988;25:423–34. http://dx.doi.org/10.2307/2403834 medical researchers, physicians, veterinarians, biologists, 13. DiSalvo AF. Blastomycosis. In: Al-Doory Y, DiSalvo AF, editors. epidemiologists, natural resource managers, and hunter and The ecology of Blastomyces dermatitidis. New York: Plenum trapper federations with the common goal of reducing dis- Medical Book Co.; 1992. p. 42–73. ease risks. 14. McIntyre L. Blastomycosis in northwestern Ontario. Can Fam Physician. 1985;31:161–4. 15. Ontario Ministry of Natural Resources. Hunting regulations summary. Acknowledgments 2013 [cited 2015 Mar 31]. https://www.ontario.ca/environment-and- We thank the veterinarians, clinicians, pathologists, biologists, energy/2013-furbearing-mammals-seasons-hr-summary and public for the submission and interpretation of blastomycosis case material, as well as the Canadian Wildlife Health Address for correspondence: Nicole M. Nemeth, Department of Cooperative colleagues for logistical support. Some case data Pathobiology, University of Guelph, 419 Gordon St, Guelph, ON were contributed by Histovet, Guelph, Ontario, Canada. N1G2W1, Canada; email: [email protected]

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